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Fish - How to ask them the right questions

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Fish represent the largest radiation of vertebrates, with over 32,000 species known to date – more than all other vertebrate species combined. While fish possess many anatomical and perceptual adaptations to the aquatic environment, most experimental procedures used to study cognition in other species are readily adaptable to fish. Their small size, ease of handling and wide range of ecological niches have made fish a model species for cognitive research for well over a century. It is impossible to do the vast literature any justice, so this chapter will focus predominantly on four model species: guppies (Poecilia reticulata), three-spined sticklebacks (Gasterosteus aculeatus) and goldfish (Carassius auratus), the most common species in cognitive research, and on zebrafish (Danio rerio), an important model organism in developmental biology and genetics that is gaining popularity in cognitive studies. In the first section of the chapter, we begin by giving an overview of some anatomical and perceptual traits of these species that are relevant to cognitive research. We then address some characteristics of their life cycle, ecology and social behavior that should be considered when studying cognition, and include some tricks for adapting cognitive tasks to this group. In the second section of the chapter, we briefly review the literature on each of the four species, giving some historical information on their use as a model species in cognition and behavior. In the last section of the chapter, we give practical examples and tips on husbandry and how to investigate spatial and social learning in fish, and how these tasks may be adapted to slightly different questions.
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... Fish have become a standard taxon in animal cognition and behavioral ecology research Vila Pouca and Brown 2018a). Many vertebrate traits are highly conserved, including brain functions and neuronal pathways (Broglio et al. 2011;Rittschof et al. 2014), making fish suitable subjects in a range of subfields, including comparative cognition, behavioral genetics, and even neuropsychiatric research (Oliveira 2013;Stewart et al. 2014). ...
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Methods for Fish Biology, 2nd edition Chapter 16: Behavior Julianna P. Kadar, Catarina Vila Pouca, Robert Perryman, Joni Pini-Fitzsimmons, Sherrie Chambers, Connor Gervais, and Culum Brown doi: https://doi.org/10.47886/9781934874615.ch16 Kadar, J. P., C. V. Pouca, R. Perryman, J. Pini-Fitzsimmons, S. Chambers, C. Gervais, and C. Brown. 2022. Pages 593–642 in S. Midway, C. Hasler, and P. Chakrabarty, editors. Methods for fish biology, 2nd edition. American Fisheries Society, Bethesda, Maryland. Humans interact with fish in a wide variety of contexts. Fish are rapidly becoming the go-to model for medical research because of the conservative nature of vertebrate physiology. We catch and grow fish in captivity for human consumption and frequently rear fish for release into the wild either to supplement wild populations to enhance fisheries or as a conservation measure. In all cases, understanding fish behavior is vital whether you are interested in stock management, conservation biology, or animal welfare (Brown 2015). Gone are the days when fish were viewed as mindless automata. We now know that fish behavior is highly flexible, providing the plasticity to allow individuals to adjust to prevailing conditions or contexts (Bshary and Brown 2014). Their level of cognitive and behavioral sophistication is on par with the rest of the vertebrates (Bshary and Schäffer 2002; Vila Pouca and Brown 2018a; 2018b). Unsurprisingly, a change in behavior is often the first sign that something has shifted in the environment; thus, behavioral studies are at the forefront of environmental and ecotoxicological research (Brown 2012; Oulton et al. 2014). The massive diversity of fishes (currently more than 32,000 described species), and the range of niches they occupy, means that generalization is nearly impossible. Thankfully, the approaches for studying fish behavior are also many and varied and rapidly developing with changes in technology. Here we provide a brief overview of some of the emerging methods for studying fish behavior. We will not be reviewing fish behavior in general since this is the topic of multiple books (e.g., Magnhagen et al. 2008; Brown et al. 2011), nor will we be providing a general overview of how to study animal behavior. Such details can readily be found in any of the many excellent texts on animal behavior or behavioral ecology (Davies 1991; Dugatkin and Earley 2004; Alcock 2005; Goodenough et al. 2009). Many people study fish behavior under captive conditions where it is possible to control the environment and observe behaviors that can be attributed to specific cognitive processes. In most instances, it is simply a matter of refining the standard methods to suit the aquatic environment and the species of interest. The main difficulties of studying fish behavior arise when trying to observe them in their natural environment. The underwater world is not a place with which most people are comfortable or familiar. Humans can stay only so long in the watery world of fishes, so many of the methods we describe here attempt to overcome these problems by studying fish behavior remotely.
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Figure 1. Feeding propensity of female guppies selected for large and small brain size when offered a novel food source (a pellet instead of flake food: 0 = never, 1 = always). Food was given once per day for 7 consecutive days. Feeding propensity is the number of times the fish ate the pellet (out of seven times). To analyse feeding propensity we used a binary general linear mixed model with feeding (yes/no) as the dependent variable, brain size treatment as a fixed factor, and replicate line, day of feeding and individual as random factors (GLMM: F = 1.945, N = 24, P = 0.176; the figure shows the mean estimated marginal means ± SE of this GLM).
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Darwin famously described special difficulties in explaining social evolution in insects. More than a century later, the evolution of sociality - defined broadly as cooperative group living - remains one of the most intriguing problems in biology. Providing a unique perspective on the study of social evolution, this volume synthesizes the features of animal social life across the principle taxonomic groups in which sociality has evolved. The chapters explore sociality in a range of species, from ants to primates, highlighting key natural and life history data and providing a comparative view across animal societies. In establishing a single framework for a common, trait-based approach towards social synthesis, this volume will enable graduate students and investigators new to the field to systematically compare taxonomic groups and reinvigorate comparative approaches to studying animal social evolution.
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Keywords: fish behaviour mirror test Poecilia reticulata shoaling sociability Many fish species are social, and individuals spend most of their lives in shoals, but sociability can vary greatly between species, populations and individuals. Sociability has been largely studied by measuring the time spent by a focal fish in proximity to one or more conspecifics. To control for the behaviour of the stimulus fish, the conspecifics have often been substituted by a mirror, on the assumption that the subject perceives its mirror image as a conspecific. The validity of the mirror test has recently been questioned, at both the behavioural and the molecular level, because of the discrepancy in fish responses when exposed to a mirror image and to a live conspecific. In this study, we compared the sociability scores of a social fish, the guppy, Poecilia reticulata, obtained using live fish or a mirror as a stimulus, to assess the validity of the mirror test. We found that the sociability score assessed using the standard mirror test was not significantly correlated with the sociability assessed using live stimuli. Nevertheless, we observed a positive correlation between the scores of the two tests when the mirror test was performed in a more naturalistic context, controlling for the minimum distance between the stimulus fish and the mirror. Our findings provide evidence of the reliability of the mirror test as a measure of so-ciability compared to the test using live conspecifics when certain requirements are satisfied.
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The effect of visible implant elastomer (VIE) tagging on the immediate physiological stress response was tested in female three-spined stickleback Gasterosteus aculeatus, using non-invasive waterborne cortisol analysis. Post-tagging cortisol levels were significantly higher compared with pretreatment baseline concentrations; however, when comparing post-tagging cortisol levels with cortisol levels after exposure to a simulated aerial predator, no significant differences were found. This study indicates that VIE tagging elicits a physiological stress response similar to those occurring in the everyday lives of this important biological model organism. © 2015 The Fisheries Society of the British Isles.
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There is a well-established tradition of studying numerical abilities in mammals and birds; however, only recently has it been proposed that some species of fish possess similar capacities. Here we review the evidence for the presence of rudimentary numerical abilities in fish. There is substantial evidence that fish can use purely numerical information both when they are trained to discriminate among different quantities and when they are required to choose which group of social companions is less/more numerous. In both contexts, however, they tend to use primarily continuous quantities (e.g., area) instead of discrete numbers when both types of information are available. Similarities among species appear greater than differences and, in general, fish numerical capacities closely match those reported in mammals and birds. The study of developmental trajectories suggests that fish have multiple core number systems that are domain-specific and serve to solve a limited set of problems.
Article
This paper describes and evaluates a flexible, non-invasive tagging system for the automated identification and long-term monitoring of individual three-spined sticklebacks Gasterosteus aculeatus. The system is based on barcoded tags, which can be reliably and robustly detected and decoded to provide information on an individual's identity and location. Because large numbers of fish can be individually tagged, it can be used to monitor individual- and group-level dynamics within fish shoals.
Article
Abstract The zebrafish offers an excellent compromise between system complexity and practical simplicity and has been suggested as a translational research tool for the analysis of human brain disorders associated with abnormalities of social behavior. Unlike laboratory rodents zebrafish are diurnal, thus visual cues may be easily utilized in the analysis of their behavior and brain function. Visual cues, including the sight of conspecifics, have been employed to induce social behavior in zebrafish. However, the method of presentation of these cues and the question of whether computer animated images versus live stimulus fish have differential effects have not been systematically analyzed. Here, we compare the effects of five stimulus presentation types: live conspecifics in the experimental tank or outside the tank, playback of video-recorded live conspecifics, computer animated images of conspecifics presented by two software applications, the previously employed General Fish Animator, and a new application Zebrafish Presenter. We report that all stimuli were equally effective and induced a robust social response (shoaling) manifesting as reduced distance between stimulus and experimental fish. We conclude that presentation of live stimulus fish, or 3D images, is not required and 2D computer animated images are sufficient to induce robust and consistent social behavioral responses in zebrafish.
Article
Migratory marine animals exploit resources in different oceanic regions at different life stages, but how they navigate to specific oceanic areas is poorly understood [1-3]. A particular challenge is explaining how juvenile animals with no prior migratory experience are able to locate specific oceanic feeding habitats that are hundreds or thousands of kilometers from their natal sites [1-7]. Although adults reproducing in the vicinity of favorable ocean currents can facilitate transport of their offspring to these habitats [7-9], variation in ocean circulation makes passive transport unreliable, and young animals probably take an active role in controlling their migratory trajectories [10-13]. Here we experimentally demonstrate that juvenile Chinook salmon (Oncorhynchus tshawytscha) respond to magnetic fields like those at the latitudinal extremes of their ocean range by orienting in directions that would, in each case, lead toward their marine feeding grounds. We further show that fish use the combination of magnetic intensity and inclination angle to assess their geographic location. The "magnetic map" of salmon appears to be inherited, as the fish had no prior migratory experience. These results, paired with findings in sea turtles [12-21], imply that magnetic maps are phylogenetically widespread and likely explain the extraordinary navigational abilities evident in many long-distance underwater migrants.
Article
One-way mirrors were used to determine whether male three-spined sticklebacks, Gasterosteus aculeatus, could use visual cues to distinguish between pairs of neighbours that had similar social and physical attributes. Neighbours were enclosed in identical tanks that had no physical landmarks. The tanks had opaque side-walls and one-way mirrors (reflecting inward) placed along end-walls; thus, neighbours could not see outside of their tanks. Neighbour tanks were positioned at the ends of a test tank so that a resident could view both neighbours. Tanks were left undisturbed until residents completed a nest (ca 4-6 days). If neighbours were then switched from one end of a residents' territory to the other, residents charged toward and bit at the neighbours more often than they did following a 'mock' switch (i.e. neighbours were moved but then returned to their original position); following actual switches, males also devoted less effort to nest maintenance. Furthermore, the amount of effort devoted to defending a given side of the tank depended on which neighbour was there. The neighbours' surroundings did not change after switches, nor did their behaviour. Thus, male sticklebacks can distinguish between familiar rivals using visual cues alone. The ability developed in 4-6 days (i.e. the time required to build nests) and did not require physical interaction with the neighbours.
Article
The view that the human mind is a repository of stored items dates at least to Aristotle and Plato and continues to dominate investigations of human memory [1]. This view fits with our intuitions that we study information as the optimal method to store information in memory and that retrieval of information functions only to assess what information was previously stored. Yet modern research on human memory suggests that retrieving information during a test facilitates later memory of that information [2-6]. Because human memory is intertwined with language, it is difficult to resist the conclusion that language is essential for this key aspect of human cognition. Here we show that practising memory retrieval improves long-term retention in a nonhuman species. We report evidence that rats' long-term memory performance is enhanced if they had previously retrieved specific items stored in memory.
Article
Laboratory-reared predator-naive three-spined sticklebacks from two sites, one with abundant predatory fish (the high-risk site) and the other essentially predator-free (the low-risk site), were given a passive avoidance conditioning task in which they received a simulated attack from a model avian predator whenever they entered a previously-favoured feeding patch. 15/16 fish learned to avoid the dangerous patch within 15 days, but those from the high-risk site did so significantly faster and received fewer attacks in the process. The two categories of fish did not differ either in active avoidance of the attack stimulus or in the rate at which they started to re-exploit the dangerous patch once negative reinforcement ceased. It is argued that fish from high- and low-risk sites differ in the negatively reinforcing properties of the same, standardised attack.
Article
Goldfish, Carassius auratus, were introduced into an arena tank containing two symmetrically placed gravel-filled trays, one of which contained hidden food. In the absence of additional structures in the tank, the accuracy of food-patch choice (i.e. the proportion of individuals contacting the full tray before the empty tray) was close to that expected assuming random binary choice. Accuracy improved significantly, however, when landmarks (a rock/plant combination or multicoloured plastic columns) were positioned close to the food patch. Choice performance also improved when the plastic columns were placed in the opposite (non-food) half of the tank, indicating a capacity for indirect landmark usage as distinct from direct visual cueing. Latencies to feeding decreased with experience in all tratments, but were significantly lower in the presence of landmarks. Exploratory sampling behaviour, as indicated by the number of visits to the empty patch once food had been found during a trial, was significantly less frequent in the presence of strong landmarks. Fish in all treatments increased the frequency of sampling visits following a reversal of full and empty patches. Reliance on memory-based spatial behaviour may therefore vary according to the nature and complexity of the visual environment.
Article
To forage efficiently in a patchy environment animals must make informed decisions concerning in which patches to forage, for which the behaviour of other animals often provides informative cues. However, other individuals may differ in the quality or relevance of information that they provide, and accordingly animals are expected to be selective with respect to whom they copy. Such selectivity may include the biasing of copying towards older, larger or more experienced conspecifics. We investigated whether the ability of nine-spined sticklebacks, Pungitius pungitius, to exploit public information, that is, to judge the relative profitability of food patches solely on the basis of the relative feeding activity of others, is influenced by their own body size and that of the individuals from whom they copy. Individual observer fish, classed as either small or large, were trained that two discrete foraging patches differed in their relative quality, one being rich and the other poor ('personal information'). They then watched two shoals of either small or large demonstrator conspecifics feeding at the two patches ('public informa- tion'), but with relative profitability of the patches reversed compared to training, before being given the opportunity to make a patch choice. The effectiveness of this public demonstration was clearly contin- gent on the size of the demonstrators, with subjects of both size classes copying the patch choice of large demonstrators significantly more than they copied the patch choice of small demonstrators. This study reinforces the view that animal social learning is directed along particular pathways, with individuals predisposed by selection to copy particular categories of individual differentially.
Article
Shoaling fish are expected, in many cases, to gain fitness benefits from being in a larger shoal and previous experiments have shown that fish are indeed capable of choosing between shoals of different sizes. We investigated the influence of shoal activity on shoal size preference in the zebrafish. We gave test fish the choice between shoals of one to four stimulus fish, presented at two different water temperatures, and so differing in their activity levels. Where all stimulus fish were in water of the same temperature, test fish generally preferred the larger shoal. However, this preference could be reduced by presenting the larger shoal in colder water and so reducing its activity. We discuss these findings with reference to the factors that may influence shoal activity, the effect of temperature on shoaling behaviour and the mechanisms that may be used by fish to discriminate shoal size.
Article
In the "standard-opponent' test the test subject fights against a much smaller opponent behind a transparent partition, whereas in the mirror test it attacks its own mirror image. When fish had been involved in a series of escalating activities without final decision of the encounters, in subsequent mirror tests their biting frequencies were elevated for at least 24h after the last fight. Winning a rank order fight led to an increase and losing to a decrease in biting frequency 24h later. After social settlement in a long-term stabilized social hierarchy the relation is totally reversed: dominant males showed much lower biting frequencies than subordinate males in the mirror test. The hypothesis is proposed that even under natural conditions high ranking males tend to use their energy potential in a more economic way than low ranking males. The existence of rank-dependent fighting strategies could be due to differences in risk: the fighting activities of dominant males are extremely risky because they can lose their high social status, which inevitably would lead to a lowered genetic fitness, whereas the aggressive actions of subordinate males are not very risky because their social status is low anyway. -from Authors
Article
Source memory is a representation of the origin (source) of information. When source information is bound together, it makes a memory episodic, allowing us to differentiate one event from another [1 • Johnson M.K. • Hashtroudi S. • Lindsay D.S. Source monitoring.Psychol. Bull. 1993; 114: 3-28 • Crossref • PubMed • Scopus (3014) • Google Scholar , 2 • Mitchell K.J. • Johnson M.K. Source monitoring 15 years later: what have we learned from fMRI about the neural mechanisms of source memory?.Psychol. Bull. 2009; 135: 638-677 • Crossref • PubMed • Scopus (386) • Google Scholar ]. Here, we asked whether rats remember the source of encoded information. Rats foraged for distinctive flavors of food that replenished (or failed to replenish) at its recently encountered location according to a source-information rule. To predict replenishment, rats needed to remember where they had encountered a preferred food type (chocolate) with self-generated (walking along a runway encountering chocolate) or experimenter-generated (placement of the rat at the chocolate site by an experimenter) cues. Three lines of evidence implicate the presence of source memory. First, rats selectively adjusted revisits to the chocolate location based on source information, under conditions in which familiarity of events could not produce successful performance. Second, source memory was dissociated from location memory by different decay rates. Third, temporary inactivation of the CA3 region of the hippocampus with lidocaine selectively eliminated source memory, suggesting that source memory is dependent upon an intact hippocampus. Development of an animal model of source memory may be valuable to probe the biological underpinnings of memory disorders marked by impairments in source memory.
Article
Previous studies have shown that guppies, Poecilia reticulata, can learn the route to a food source by shoaling with knowledgeable conspecifics, and prefer to shoal with experienced foragers and familiar fish. We tested the hypothesis that guppies would learn more effectively from (1) familiar than unfamiliar demonstrators and (2) well-trained than poorly trained demonstrators. Demonstrator fish were given experience in swimming a route to a food source and then introduced into shoals of untrained observer guppies; the spread of this foraging skill was recorded over 15 trials. The demonstrators were either familiar or unfamiliar to the observers and either well trained or poorly trained. Observers performed significantly better when the demonstrators were familiar. The training of the demonstrators made no overall difference to the performance of naıve observers. However, whilst observers in shoals exposed to well-trained demonstrators did better initially than those with poorly trained ones, the latter learned the route to the feeder faster. Our results suggest that familiarity may generate a form of directed social learning in guppy shoals, in which fish learn more effectively from familiar conspecifics. An analysis of who follows whom suggests that well-trained demonstrators can provide a ‘tip-off’ as to the location of the hole but poorly trained demonstrators were more likely to be followed. The results suggest that while observers are able to shoal with poorly trained demonstrators, well-trained demonstrators swim the maze route too quickly to be followed, but may attract attention to the maze route.